Large differences in thermal tolerance between isolated organs in rainbow trout

Leon Michael Pfeufer , Catharina Olsson, Fredrik Jutfelt 

Due to climate change, research on thermal performance limits in ectotherms has received much attention in the last two decades. However, the underlying physiological mechanisms and most vulnerable organs remain largely unknown. Here, we examined contractile performance in different organs from rainbow trout during an acute warming challenge, including the heart (cardiac muscle), caudal peduncle (white skeletal muscle) and the gastrointestinal tract (smooth muscle). The preparations were electrically stimulated at three voltages in vitro to record contraction force, while temperature was progressively increased. To relate tissue-level responses to organismal thermal limits, whole-animal thermal tolerance (CTmax) was recorded. White skeletal muscle was the most vulnerable, retaining less than 25% of baseline contraction force at the whole-animal CTmax temperature. This suggests that white skeletal muscle may be a previously overlooked contributor to acute upper thermal limits in fish. Notably, skeletal muscle contraction force had already fallen to 50% of baseline several degrees below CTmax, indicating that heat waves may impair swim performance well below lethal thermal limits. Additionally, only 50% of the atrial preparations still produced spontaneous contractions at CTmax temperature, suggesting severe impairment of excitation-contraction coupling at high temperatures. We observed a voltage-dependent decline in ventricular contractility, consistent with predictions of the temperature-dependent deterioration of electrical excitability (TDEE) hypothesis, whereas no comparable voltage-dependent pattern was observed in white skeletal muscle. This suggests that reduced electrical excitability at elevated temperatures is not universal across electrically excitable tissues. Together, our results identify white skeletal muscle and cardiac function as potential contributors to acute upper thermal tolerance limits.